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Galati DF, Abuin DS, Tauber GA, et al. Automated image analysis reveals the dynamic 3-dimensional organization of multi-ciliary arrays. Biol Open. 2015;5(1):20-31doi: 10.1242/bio.014951.
Galati, D. F., Abuin, D. S., Tauber, G. A., Pham, A. T., & Pearson, C. G. (2015). Automated image analysis reveals the dynamic 3-dimensional organization of multi-ciliary arrays. Biology open, 5(1), 20-31. https://doi.org/10.1242/bio.014951
Galati, Domenico F, et al. "Automated image analysis reveals the dynamic 3-dimensional organization of multi-ciliary arrays." Biology open vol. 5,1 (2015): 20-31. doi: https://doi.org/10.1242/bio.014951
Galati DF, Abuin DS, Tauber GA, Pham AT, Pearson CG. Automated image analysis reveals the dynamic 3-dimensional organization of multi-ciliary arrays. Biol Open. 2015 Dec 23;5(1):20-31. doi: 10.1242/bio.014951. PMID: 26700722; PMCID: PMC4728305.
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Biol Open. 2015 Dec 23;5(1):20-31. doi: 10.1242/bio.014951.

Automated image analysis reveals the dynamic 3-dimensional organization of multi-ciliary arrays.

Biology open

Domenico F Galati, David S Abuin, Gabriel A Tauber, Andrew T Pham, Chad G Pearson

Affiliations

  1. Department of Cell and Developmental Biology, University of Colorado School of Medicine, 2801 East 17th Ave, Aurora, CO 80045-2537, USA [email protected] [email protected].
  2. Department of Cell and Developmental Biology, University of Colorado School of Medicine, 2801 East 17th Ave, Aurora, CO 80045-2537, USA.

PMID: 26700722 PMCID: PMC4728305 DOI: 10.1242/bio.014951

Abstract

Multi-ciliated cells (MCCs) use polarized fields of undulating cilia (ciliary array) to produce fluid flow that is essential for many biological processes. Cilia are positioned by microtubule scaffolds called basal bodies (BBs) that are arranged within a spatially complex 3-dimensional geometry (3D). Here, we develop a robust and automated computational image analysis routine to quantify 3D BB organization in the ciliate, Tetrahymena thermophila. Using this routine, we generate the first morphologically constrained 3D reconstructions of Tetrahymena cells and elucidate rules that govern the kinetics of MCC organization. We demonstrate the interplay between BB duplication and cell size expansion through the cell cycle. In mutant cells, we identify a potential BB surveillance mechanism that balances large gaps in BB spacing by increasing the frequency of closely spaced BBs in other regions of the cell. Finally, by taking advantage of a mutant predisposed to BB disorganization, we locate the spatial domains that are most prone to disorganization by environmental stimuli. Collectively, our analyses reveal the importance of quantitative image analysis to understand the principles that guide the 3D organization of MCCs.

© 2016. Published by The Company of Biologists Ltd.

Keywords: Automated image analysis; Basal body; Centriole; Cilia; Poc1; Polarity; Tetrahymena

References

  1. Science. 2006 Feb 3;311(5761):629-32 - PubMed
  2. Mol Biol Cell. 2006 Sep;17(9):4069-79 - PubMed
  3. J Cell Biol. 2014 Dec 22;207(6):705-15 - PubMed
  4. J Embryol Exp Morphol. 1959 Jun;7:241-56 - PubMed
  5. J Cell Biol. 1969 Mar;40(3):716-33 - PubMed
  6. Mol Biol Cell. 2005 Aug;16(8):3606-19 - PubMed
  7. Science. 1967 Oct 27;158(3800):527 - PubMed
  8. Exp Cell Res. 1975 Feb;90(2):345-56 - PubMed
  9. Annu Rev Cell Dev Biol. 2004;20:677-93 - PubMed
  10. Methods Appl Fluoresc. 2015 Mar;3(1):014003 - PubMed
  11. J Eukaryot Microbiol. 1995 Jul-Aug;42(4):422-7 - PubMed
  12. J Cell Sci. 2013 Apr 1;126(Pt 7):1659-71 - PubMed
  13. J Cell Biol. 2009 Dec 14;187(6):905-20 - PubMed
  14. Mol Biol Cell. 2009 Feb;20(3):904-14 - PubMed
  15. J Cell Biol. 2011 Oct 3;195(1):19-26 - PubMed
  16. Trends Genet. 2011 Aug;27(8):307-15 - PubMed
  17. Annu Rev Physiol. 2015;77:379-406 - PubMed
  18. Methods Cell Biol. 2012;109:393-410 - PubMed
  19. Cell. 2009 May 15;137(4):672-84 - PubMed
  20. Proc Natl Acad Sci U S A. 2005 Feb 1;102(5):1419-23 - PubMed
  21. Dev Biol. 1971 Oct;26(2):296-305 - PubMed
  22. J Cell Sci. 1996 Dec;109 ( Pt 13):3089-102 - PubMed
  23. J Neurosci. 2014 Apr 30;34(18):6377-88 - PubMed
  24. J Cell Sci. 2007 Sep 1;120(Pt 17):3075-85 - PubMed
  25. EMBO J. 2009 Feb 4;28(3):223-33 - PubMed
  26. Nat Cell Biol. 2013 Dec;15(12):1434-44 - PubMed
  27. Nat Cell Biol. 2006 Jun;8(6):581-5 - PubMed
  28. Curr Biol. 2009 Apr 28;19(8):694-9 - PubMed
  29. Eukaryot Cell. 2008 Oct;7(10):1617-39 - PubMed
  30. Am J Respir Crit Care Med. 1996 Mar;153(3):1123-9 - PubMed
  31. Genetics. 1988 Oct;120(2):389-95 - PubMed
  32. Methods Cell Biol. 2000;62:27-125 - PubMed
  33. BMC Bioinformatics. 2010 May 21;11:274 - PubMed
  34. J Cell Biol. 1975 Jun;65(3):503-12 - PubMed
  35. Nature. 2007 May 3;447(7140):97-101 - PubMed
  36. Science. 2014 Nov 14;346(6211):857-60 - PubMed
  37. J Cell Sci. 2014 Jul 1;127(Pt 13):2803-10 - PubMed
  38. Dev Biol. 1995 Jun;169(2):644-61 - PubMed
  39. Development. 2013 Aug;140(16):3468-77 - PubMed
  40. J Exp Zool. 1973 Jun;184(3):365-8 - PubMed
  41. J Cell Biol. 2009 Jun 29;185(7):1135-48 - PubMed
  42. Development. 1993 Aug;118(4):1255-66 - PubMed
  43. Dev Cell. 2013 Oct 14;27(1):103-12 - PubMed
  44. Nat Genet. 2008 Jul;40(7):871-9 - PubMed
  45. J Exp Zool. 1964 Apr;155:403-35 - PubMed
  46. Curr Opin Cell Biol. 2008 Feb;20(1):48-52 - PubMed
  47. J Cell Sci. 2013 Aug 1;126(Pt 15):3441-51 - PubMed
  48. J Protozool. 1974 Oct;21(4):549-51 - PubMed
  49. Cell. 1998 Dec 11;95(6):829-37 - PubMed
  50. J Histochem Cytochem. 1977 Jul;25(7):741-53 - PubMed
  51. Traffic. 2009 May;10(5):461-71 - PubMed
  52. J Protozool. 1967 Nov;14(4):553-65 - PubMed
  53. Mol Biol Cell. 2012 Dec;23(24):4820-32 - PubMed
  54. J Protozool. 1978 Feb;25(1):113-9 - PubMed
  55. J Exp Zool. 1978 Jun;204(3):417-30 - PubMed
  56. J Cell Biol. 1978 Dec;79(3):727-36 - PubMed
  57. Cell. 2008 Nov 28;135(5):894-906 - PubMed
  58. Bioinformatics. 2013 Jul 15;29(14):1840-1 - PubMed
  59. Proc Natl Acad Sci U S A. 2013 Mar 19;110(12):4470-5 - PubMed
  60. Nat Rev Mol Cell Biol. 2011 Apr;12(4):222-34 - PubMed

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